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SCIENCE ADVANCES | RESEARCH ARTICLE EVOLUTIONARY BIOLOGY Copyright © 2021 The Authors, some rights reserved; The evolution of mammalian brain size exclusive licensee J. B. Smaers1,2*, R. S. Rothman3, D. R. Hudson3, A. M. Balanoff4,5, B. Beatty6,7, D. K. N. Dechmann8,9, American Association 10 11,12,13 14 6,15,16,17 18 19 for the Advancement D. de Vries , J. C. Dunn , J. G. Fleagle , C. C. Gilbert , A. Goswami , A. N. Iwaniuk , of Science. No claim to 14,20 12 21,22,23,24 25 2,3,26 W. L. Jungers , M. Kerney , D. T. Ksepka , P. R. Manger , C. S. Mongle , original U.S. Government 1 23,27 28 29 8,9 F. J. Rohlf , N. A. Smith , C. Soligo , V. Weisbecker , K. Safi Works. Distributed under a Creative Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental Commons Attribution role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selec- NonCommercial tion on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling License 4.0 (CC BY-NC). relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mammalian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size. Downloaded from INTRODUCTION It has long been recognized that brain size scales with body size The brain is directly responsible for governing an animal’s interac following a standard linear allometric power law (6). The scaling tions with its environment. As such, the brain is often considered to coefficient (slope) of this allometry is assumed to be relatively stable flexibly respond to selection in changing environments (1–3). Brain across vertebrate classes and orders (most often estimated as be http://advances.sciencemag.org/ size is, however, also commonly accepted to be restrained by ener tween 2/3 and 3/4) (7) and is thought to reflect universal energetic getic requirements that are considered universal across all verte growth constraints (4, 5). Largely because of methodological limita brates (4, 5). This apparent paradox highlights that brain size is one tions in phylogenetic comparative statistics, this working hypo of the most salient traits for understanding the fundamental balance thesis has received little scrutiny. Previous studies have therefore between adaptability and constraint in evolution. Despite this im mostly been limited to comparing residual variation along a stable portance, crucial aspects related to the timing, pattern, and drivers slope [i.e., mean relative brain size or encephalization quotient that underlie modern phenotypic diversity in brain size remain (EQ), quantified through differences in the intercept of the evolu undescribed. tionary allometry] (7, 8). There is, however, evidence to suggest that changes in the slope (quantifying changes in brainbody covaria 1 tion) may constitute an important additional source of comparative Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA. on April 28, 2021 2Division of Anthropology, American Museum of Natural History, New York, variation (9–12). 3 NY 10024, USA. Interdepartmental Doctoral Program in Anthropological Sciences, Identifying the points at which evolutionary shifts in brainbody Stony Brook University, Stony Brook, NY 11794, USA. 4Department of Psychologi- cal and Brain Sciences Johns Hopkins University, Baltimore, MD 21218, USA. 5Division covariation occur is of paramount importance to understanding the of Paleontology, American Museum of Natural History, New York, NY 10024, USA. selection pressures that may be operating. Whereas shifts in inter 6NYIT College of Osteopathic Medicine, Old Westbury, NY 11568, USA. 7United cept address changes in mean among traits, shifts in slope address States National Museum, Smithsonian Institution, Washington, DC 20560, USA. 8 changes in variation among traits (e.g., stabilizing selection restrains Department of Migration, Max-Planck Institute of Animal Behavior, 78315 Radolfzell, Germany. 9Department of Biology, University of Konstanz, 78464 Konstanz, Germany. variation, divergent selection allows for variation) (13). Failing to 10Ecosystems and Environment Research Centre, School of Science, Engineering account for the possibility that trait covariation may differ among 11 and Environment, University of Salford, Manchester M5 4WX, UK. Division of Bio- groups of species could potentially hide crucial sources of variation logical Anthropology, University of Cambridge, Cambridge CB2 3QG, UK. 12Behav- ioral Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK. that contribute to explaining phenotypic diversity. Moreover, evo 13Department of Cognitive Biology, University of Vienna, Vienna 1090, Austria. lutionary allometries (allometries quantified across species) are de 14Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY termined by ontogenetic and static allometries (across developmental 11794, USA. 15Department of Anthropology, Hunter College, New York, NY 10065, USA. 16PhD Program in Anthropology, Graduate Center of the City University of time in the same individual and individuals of the same species, New York, 365 Fifth Avenue, New York, NY 10016, USA. 17New York Consortium in Evo- respectively) and thus are indicative of the genetic and developmen lutionary Primatology, New York, NY 10065, USA. 18Department of Life Sciences, Nat- tal mechanisms that regulate growth (14). Consequently, more de 19 ural History Museum, London SW7 5BD, UK. Department of Neuroscience, tailed information on the allometric patterns that characterize the University of Lethbridge, Lethbridge, AB T1K-3M4, Canada. 20Association Vahatra, BP 3972, Antananarivo 101, Madagascar. 21Bruce Museum, Greenwich, CT 06830, USA. brainbody relationship across evolutionary time will provide new 22Department of Ornithology, American Museum of Natural History, New York, NY opportunities to investigate the nature of the processes that shape 23 10024, USA. Division of Science and Education, Field Museum of Natural History, those patterns. Last, the occurrence of shifts in slope would indicate Chicago, IL 60605, USA. 24Department of Paleobiology, Smithsonian Institution, Washington, DC 20013, USA. 25School of Anatomical Sciences, Faculty of Health that comparisons of relative brain size (and EQ) are only valid among Sciences, University of the Witwatersrand, Johannesburg, South Africa. 26Turkana groups with a similar slope. The ubiquitous approach of quantify Basin Institute, Stony Brook University, Stony Brook, NY 11794, USA. 27Campbell ing only residual variation along a stable slope may therefore lead to Geology Museum, Clemson University, Clemson, SC 29634, USA. 28Department of 29 biased results and incorrect interpretations. Anthropology, University College London, London WC1H 0BW, UK. College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia. Birds and mammals are of particular interest in this context be *Corresponding author. Email: [email protected] cause they both independently evolved relatively larger brains than Smaers et al., Sci. Adv. 2021; 7 : eabe2101 28 April 2021 1 of 11 SCIENCE ADVANCES | RESEARCH ARTICLE other vertebrate classes (7). This innovation was likely facilitated by boundary (~23 Ma ago), after which several significant shifts oc an easing of the phenotypic integration between brain size and body curred rapidly (Table 1 and table S2). These shifts from the ances size (15). Such decoupling leads to increased variation available to tral grade (slope: b = 0.51) resulted in new slopes for colobines selection, which, in turn, is expected to heighten flexibility in re (b = 0.67), cercopithecines (b = 0.43), lesser apes (b = 0.32), great sponse to selection (16). Recent work has shown that shifts in slope apes (b = 0.23), hominins (b = 1.10), and callitrichines (b = 0.58). are paramount to explaining the brain’s evolutionary diversification Other shifts in slope near the PaleogeneNeogene boundary oc in birds (12), demonstrating that the selective response to increased curred in bears and pinnipeds (Fig. 1; Table 1 and table S2), which variation is not restricted solely to changes in mean relative brain are noteworthy for having the largest downward shifts in slope in size but may also play out in terms of changes in brainbody covari the sample: from b = 0.58 in other carnivorans to b = 0.39 and ation. In mammals, shifts in brainbody covariation have been sug b = 0.23, respectively. See the Supplementary Results for a complete gested to occur in primates (9), carnivorans (17), marsupials, (18), description of allometric repatterning across clades. and among mammalian orders (11). However, it has remained un clear where and when such shifts occur throughout mammalian evolution and how they contribute to explaining variation in the DISCUSSION brainbody relationship. Different evolutionary trajectories for the Several methodological innovations (19,

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